Shifts in microbial community composition and metabolism correspond with rapid soil carbon accumulation in response to 20 years of simulated nitrogen deposition

Anthropogenic nitrogen (N) deposition and fertilization in boreal forests frequently reduces decomposition and soil respiration and enhances C storage in the topsoil. This enhancement of the C sink can be as strong as the aboveground biomass response to N additions and has implications for the global C cycle, but the mechanisms remain elusive. We hypothesized that this effect would be associated with a shift in the microbial community and its activity, and particularly by fungal taxa reported to be capable of lignin degradation and organic N acquisition. We sampled the organic layer below the intact litter of a Norway spruce (Picea abies (L.) Karst) forest in northern Sweden after 20 years of annual N additions at low (12.5 kg N ha−1 yr−1) and high (50 kg N ha−1 yr−1) rates. We measured microbial biomass using phospholipid fatty-acid analysis (PLFA) and ergosterol measurements and used ITS metagenomics to profile the fungal community of soil and fine-roots. We probed the metabolic activity of the soil community by measuring the activity of extracellular enzymes and evaluated its relationships with the most N responsive soil fungal species. Nitrogen addition decreased the abundance of fungal PLFA markers and changed the fungal community in humus and fine-roots. Specifically, the humus community changed in part due to a shift from Oidiodendron pilicola, Cenococcum geophilum, and Cortinarius caperatus to Tylospora fibrillosa and Russula griseascens. These microbial community changes were associated with decreased activity of Mn-peroxidase and peptidase, and an increase in the activity of C acquiring enzymes. Our results show that the rapid accumulation of C in the humus layer frequently observed in areas with high N deposition is consistent with a shift in microbial metabolism, where decomposition associated with organic N acquisition is downregulated when inorganic N forms are readily available.